A NEW RECORD OF THE EVORON VOLE (RODENTIA, ARVICOLINAE:ALEXANDROMYS EVORONENSIS) IN THE FAR EAST Текст научной статьи по специальности «Биологические науки»

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AMypcKuu зооAогинескиu rnypnaA, 2023, m. XV, № 2

Amurian Zoological Journal, 2023, vol. XV, no. 2

www.azjournal.ru

# Ch kf Ht https://www.doi.org/10.33910/2686-9519-2023-15-2-378-384

http://zoobank.org/References/A9AC8129-DD10-4488-8C18-A1073B91F62A

UDC 599.323.43

A new record of the Evoron vole (Rodentia, Arvicolinae: Alexandromys evoronensis) in the Far East

I. V. Kartavtseva1H, A. I. Stepanova1, I. N. Sheremetyeva1, M. V. Pavlenko1, L. V. Frisman2

1 Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, 159 Stoletiya Vladivostoka Ave., 690022, Vladivostok, Russia 2 Institute for Complex Analysis of Regional Problems, Far Eastern Branch of the Russian Academy of Sciences,

4 Sholom-Aleichema Str., 679016, Birobidzhan, Russia

Authors

Irina V. Kartavtseva

E-mail: Kartavts [email protected]

SPIN: 8486-5612

Scopus Author ID: 6603816919

ResearcherID: M-2403-2016

ORCID: 0000-0003-2136-8253

Anastasia I. Stepanova E-mail: [email protected]

Irina N. Sheremetyeva E-mail: [email protected] SPIN: 4490-5584 Scopus Author ID: 6504016204 ResearcherID: L-9392-2016 ORCID: 0000-0003-3464-9009 Marina V. Pavlenko E-mail: mv [email protected] SPIN: 2149-2274 Scopus Author ID: 35808905800 ORCID: 0000-0002-7772-7019 Liubov V. Frisman E-mail: [email protected] SPIN: 5244-3989 Scopus Author ID: 7003582229 ResearcherID: J-9165-2018 ORCID: 0000-0002-4674-5978

Abstract. Alexandromys evoronensis is the endemic vole of the Russian Far East. The range of the species is still unclear. Previously, this species was found in two intermontane areas of the Khabarovsk Krai and one area of the Amur Oblast. We recorded this species in a new location in August 2021 and August 2022. It is a small intermountain area of the western spurs of the Bureinsky Range, in the Tyrma River valley, Khabarovsk Krai (50°01'17.55''N, 132°03'02.60"E). A total of eight Evoron voles were caught here. Karyotyping of one female (2n = 36) revealed a similarity with the karyotype of the Argi chromosomal race of the A. evoronensis. New records of the voles in the Tyrma River valley expand the range of Evoron vole and indicate more southerly habitats than previously stated.

Copyright: © The Authors (2023). Published by Herzen State Pedagogical

University of Russia. Open access under Keywords: Russian Far East, fauna, Evoron vole, new findings, new record, CC BY-NC License 4.0. karyotype

Новая находка эворонской полевки Alexandromys evoronensis (Rodentia, Arvicolinae) на Дальнем Востоке

И. В. Картавцеваш, А. И. Степанова1, И. Н. Шереметьева1, М. В. Павленко1, Л. В. Фрисман2

1 Федеральный научный центр биоразнообразия наземной биоты Восточной Азии ДВО РАН,

пр-т 100-летия Владивостока, д. 159, 690022, г. Владивосток, Россия

2 Институт комплексного анализа региональных проблем Дальневосточного отделения РАН,

ул. Шолом-Алейхема, д. 4, 679016, г. Биробиджан, Россия

Сведения об авторах Картавцева Ирина Васильевна E-mail: [email protected] SPIN-код: 8486-5612 Scopus Author ID: 6603816919 ResearcherlD: M-2403-2016 ORCID: 0000-0003-2136-8253

Степанова Анастасия Игоревна E-mail: [email protected] om

Шереметьева Ирина Николаевна E-mail: [email protected] SPIN-код: 4490-5584 Scopus Author ID: 6504016204 ResearcherID: L-9392-2016 ORCID: 0000-0003-3464-9009 Павленко Марина Владимировна E-mail: mv [email protected] SPIN-код: 2149-2274 Scopus Author ID: 35808905800 ORCID: 0000-0002-7772-7019

Фрисман Любовь Васильевна E-mail: [email protected] SPIN-код: 5244-3989 Scopus Author ID: 7003582229 ResearcherID: J-9165-2018 ORCID: 0000-0002-4674-5978

Права: © Авторы (2023). Опубликовано Российским государственным педагогическим университетом им. А. И. Герцена. Открытый доступ на условиях лицензии CC BY-NC 4.0.

Аннотация. Л1ехап4готуз егогопет18 — эндемик Дальнего Востока России. Ареал вида все еще не ясен. Ранее этот вид был обнаружен в двух межгорных районах Хабаровского края и одном в Амурской области. Мы обнаружили этот вид в новой точке: небольшой межгорной долине реки Тырма западных отрогов Буреинского хребта, Хабаровском крае (50°01'17.55'' с. ш., 132°03'02.60'' в. д.) в августе 2021 и 2022 гг. Всего здесь поймано восемь особей эворонской полевки. Кариотипирование одной самки (2п = 36) выявило сходство с кариотипом хромосомной расы "Лщ" этого вида. Нахождение полевок в долине р. Тырма расширяет ареал эворонской полевки и указывает на более южные места обитания.

Ключевые слова: Дальний Восток России, фауна, эворонская полевка, новые находки, кариотип

Introduction

The Evoron vole Alexandromys evoronen-sis (Kovalskaya et Sokolov, 1980) is the endemic vole found in the south of the Russian Far East. The species is unusual in multiple structural chromosomal rearrangements — both tandem and centromeric fusions are in a heterozygous state. Eleven chromosomes — seven acrocentrics (A) and four metacentrics (M) — are involved in multiple structural rearrangements with the formation of 20 variants of karyotypes (Kartavtseva et al. 2021a). It has been suggested that the species is at the stage of speciation that is accompanied by multiple rearrangements — a rare case these days (Kartavtseva et al. 2021a).

The species was first described from a population No I (Fig. 1: A) of Evoron-Chukchagir

lowland, Lake Evoron valley in the Khabarovsk Krai, Russian Far East, according to morphological, chromosomal (2n = 38-40, NF = 5258) and hybridological comparisons with morphologically related species (Kovalskaya, Sokolov 1980). Later, these characteristics were reviewed — 2n = 38-41, NF = 54-59 (Kartavtseva et al. 2021a).

Recently, two more isolated populations No II and No III in of the species were found in the two intermountain areas of the Russian Far East: the Verkhnebureinskaya Depression in the Khabarovsk Krai (population No II) and the Verkhnezeya Plain in the Amur Oblast (population No III) (Fig. 1: A) (Sheremetyeva et al. 2017a; 2017b).

Differential staining of animal chromosomes from the two new localities showed

Рис. 1. Карта мест сбора, внешний вид Alexandromys evoronensis и кариотип. (A) Черные кружки соответствуют хромосомной расе «Эворон»; черные звездочки — хромосомной расе «Арги» (Kartavtseva et al. 2021a; 2021b). Популяции, расположенные в межгорных районах юга Дальнего Востока России: I — Эворон-Чукчагирская низменность; II — Верхнебуреинская впадина; III — Верхнезейская равнина. Ряды пунктирных линий обозначают горные хребты. (B) — заболоченная низменность поросшая разнотравьем, дерновые луга с небольшими участками широколиственных лесов долины р. Тырма, 7 августа 2022 г. (С) Фотография эворонской полевки (№ 4700 $). (D) Кариотип эворонской полевки (№ 4700 $): 2n = 36, NF = 56, M-Sm - метацентрики-субметецентрики, А — акроцентрики, С — хромосомы разной морфологии, образованные в результате слияния акроцентрических хромосом двумя типами: центромера-центромера (13.15, 17.18) и центромера-теломера (11/19).

Fig. 1. The map of the collection localities, appearance of the Alexandromys evoronensis and its karyotype. (A) Black circles correspond to the Evoron chromosomal race; black stars to the Argi chromosomal race (Kartavtseva et al. 2021a; 2021b). Populations located in the intermontane regions of the south of the Far East: I — Evoron-Chukchagirskaya Lowland; II — Verkhnebureinskaya Depression; III — Verkhnezeiskaya Plain. Rows of dotted lines indicate mountain ranges. (B) The swampy lowland overgrown with grass, sod meadows with small areas of broad-leaved forests of the Tyrma River valley, August 7, 2022. (С) An image of Evoron vole (No 4700 $). (D) The karyotype of Evoron vole (No 4700): 2n = 36, NF = 56, M-Sm — metacentrics-submetecenrtics, A — acrocentrics, C — chromosomes of different morphology formed as a result of fusion of acrocentric chromosomes of two types: centromere-centromere (13.15, 17.18) and centromere-telomere (11/19)

their similarity in the number of chromosomes and the nature of chromosome variability (2n = 34, 36, 37, NF = 51-56). They were named the "Argi" chromosomal race. Individuals with the maximum number (2n = 38-41, NF = 54-59) from terra typica were named the Evoron chromosomal race (Kartavtseva et al. 2021b).

The nine chromosomes: two metacen-trics (No 6 and No 7) and seven acrocentrics (Nos 11, 13, 14, 15, 17, 18 and 19) of the Argi chromosomal race are involved in two types of structural rearrangements. The first rearrangement is a tandem fusion (Nos 11/19 A, 13/15 A, 17/18 A, 6/7/14 submetacentrics (Sm)). The second is a Robertsonian translocation with the formation of two metacen-trics (Nos 13.15 and Nos 17.18). The karyo-type with 2n = 34 with a rare tandem fusion of three autosomes — two meta-submetacen-trics (No 6 and No 7) and one acrocentric (No 14) — forms a large biarmed chromosome (Nos 6/7/14 Sm). Most chromosomes are heterozygous except for chromosome 11/19.

Only four chromosomes of the Evoron chromosomal race area involved in chromosomal rearrangements (1 M, 4M, 17 A, 18 A). The tandem fusion (1/4 Sm) was found in this

chromosomal race only (Kartavtseva et al. 2021a).

The study of mt DNA (Sheremetyeva et al. 2023) showed a low level of genetic differentiation of the three populations (I - III) however, the new population (IV) of this species requires further research to understand interpopulation variability.

To date, there is no data on the distribution boundaries of the species. Each new discovery of individuals belonging to this species contributes to the knowledge about the species and its morphological and genetic features. The reported study focuses on new records of the Evoron vole in a previously unexplored region and describes its karyotype. The characteristics of the karyotype made it possible to confidently attribute the individuals under study to the Evoron vole.

Material and methods

In total, eight voles were caught from the natural population of voles in the Tyrma River valley, Verkhnebureinsky District, Khabarovsk Krai (Fig. 1: A, Table 1 and Table 2). Our location was along the road running along the left bank of the river from the village Tyrma to the village Alanap (population IV, Argy - TR).

Таблица 1

Характеристика промеров тела (в мм) особей Alexandromys evoronensis, отловленных в 2021-2022 гг. в долине р. Тырма

Table 1

Body measurements (mm) of Alexandromys evoronensis specimens caught in 20212022 in the Tyrma River valley

Year/ Год Collection number/ Зоологический номер Sex/ Пол Age/ Возраст Body length / длина тела Tail length / длина хвоста Foot length длина/ ступни Ear length/ длина уха Tail-to-body length ratio, %/ Соотношение длины тела к длине хвоста

2022 4766 ? sad 100 30 20 13 33.3

2022 4793 â ad 123 47 23 15 26.2

2022 4798 â ad 132 57 19 14 23.2

2022 4799 ? ad 132 52 20 17 25.4

2022 4800 ? ad 136 46 21 15 29.7

2022 4803 â ad 124 43 21 18 28.8

2021 4804 ? ad 115 _ 22 15 —

2021 9-22 ? ad 113 48 20 13 23.5

Таблица 2

Промеры тела (мм, средние числа (min - max)), хромосомных рас Alexandromys

evoronensis из четырех популяций

Table 2

Body measurements (mm, average (min - max)) of Alexandromys evoronensis from

four populations

Популяция «Хромосомная раса» Локалитет/ Population Chromosomal race Locality Number of animals Body length / длина тела Tail length / длина хвоста Foot length длина/ ступни Ear length / длина уха Tail-to-body length ratio / Соотношение длины тела к длине хвоста (%) Source/ Источник

I Evoron — PO (52°25.42''N, 136°29.67''E) 39 141.26 (108-167) 58.66 (38-73) 19.82 (18-22) 14.24 (12-18) 23.96 Kartavtseva et al. 2022

II Argy — UG (51°05'54.49''N, 132°33'04.79''E) 6 130.50 (109-144) 53.00 (37-58) 21.17 (20-22) 14.83 (12-17) 26.4 Kartavtseva et al. 2022

III Argy — AG (54°40'10.62''N, 129°06'39.73''E) 54 137.15 (100-162) 54.00 (34-74) 19.32 (12-24) 14.14 (11-19) 26.05 Kartavtseva et al. 2022

IV Argy — TR (50°01'17.55''N, 132°03'02.60''E) 7 125 (113-136) 48.8 (43-57) 20.8 (19-23) 15.2 (13-18) 26.1 Our data/ Наши данные

In 2021, (Fig. 1: B), we caught 2? voles (set 162 Sherman traps). In 2022, we caught six voles (3^ and 3?) (set 353 Sherman traps). One female (Fig. 1: C) was karyotyped (No 4800). Standard measurements of the body of eight animals studied for the first time are given in Table 1. The comparison of body measurements of voles was carried out for the two chromosomal races studied previously (Kartavtseva et al. 2022) from three (I—III) geographic populations (Fig. 1: A): I — chromosomal race Evoron —PO; II — chromosomal race Argy — UG, III — chromosomal race Argy — AG. For body measurement see Table. 2. The first word in the quotation marks means the name of the chromosomal race, the two capital letters mean the locality (PO — the Polina Osipenko Village, UG — the Urgal River, AG — the Argi River, TR — the Tyrma River).

Chromosome preparations were prepared under laboratory conditions according to the standard method from bone marrow. Meta-

phase plates were analyzed using an Axio Imager 1 microscope at the Center for Collective Use of the Federal Scientific Center for Biodiversity, Far East Branch, Russian Academy of Sciences.

Results and discussion

The karyotype with 2n = 36, NF = 56 (Fig. 1: D) contains 18 biarmed and 16 acrocentric autosomes. The X chromosome is a medium-sized submetacentric. This karyotype corresponds to the Evoron vole of the Argi race (Kartavtseva et al. 2021a). Chromosome numbers are assigned according to the previously published data for voles with 36 chromosomes: karyotype 2n = 36b. Without differential staining of chromosomes, we cannot confidently state which chromosomes underwent structural rearrangements and the type of these rearrangements.

Body measurements of the Evoron vole from four populations (Table 2 and Fig. 2) show two groupings. The first group includes

Рис. 2. Классификация выборок (I - IV) Alexandromys evoronensis по данным промеров тела методом UPGMA.

Fig. 2. Classification of Alexandromys evoronensis (I - IV) using UPGMA body measurements (given in Euclidean distances)

populations I and III, the second populations II and IV. Population IV studied by us for the first time is similar to population II. The Tyrma and Urgal rivers (population II) originate in the southwestern slopes of the Bureinsky Range and flow into the Bu-reya River (Fig. 1: A). In the lower reaches, the Tyrma River makes a sharp bend, inside which swampy lowlands overgrown with grass and tussock meadows with small areas of broad-leaved forests predominate (Fig. 1: B). Both populations (II and IV) are located in the western spurs of the Bureinsky Range. These populations may have a common origin.

However, drawing the conclusion about the similarity of populations with those stud-

ied previously requires further morphological and genetic investigation. Karyotyping of one female (2n = 36) revealed a similarity with the Argi chromosomal race of the A. evoron-ensis (karyotype 36 = 36b) from populations II and III. The new records of voles in the Tyrma River valley expand the range of Evoron vole and indicates more southerly habitats than previously stated.

Funding

The study is part of the state-commissioned assignment of the Ministry of Science and Higher Education of the Russian Federation (No 121031500274-4 "Evolutionary aspects of the formation of the terrestrial biota of East Asia").

References

Kartavtseva, I. V., Sheremetyeva, I. N., Pavlenko, M. V. (2021a) Intraspecies multiple chromosomal variations including rare tandem fusion in the Russian Far Eastern endemic evoron vole Alexandromys evoronensis (Rodentia, Arvicolinae). Comparative Cytogenetics, vol. 15, no. 4, pp. 393-411. https:// doi.org/10.3897/compcytogen.v15.i4.67112 (In English) Kartavtseva, I. V., Sheremetyeva, I. N., Pavlenko, M. V. (2021b) Multiple chromosomal polymorphism of "evoron" chromosomal race of the evoron vole (Rodentia, Arvicolinae)]. Russian Journal of Genetics, vol. 57, no. 1, pp. 70-82. https://doi.org/10.1134/S1022795421010087 (In English) Kartavtseva, I. V., Stepanova, A. I., Sheremetyeva, I. N. et al. (2022) Novye dannye o krasnoknizhnom vide Khabarovskogo kraya — evoronskoj polevke Alexandromys evoronensis (Rodentia, Arvicolinae) [The latest data concerning the endangered species in Khabarovsk region — evoron vole

Alexandromys evoronensis (Rodentia, Arvicolinae)]. In: V. V. Rozhnov (ed.). Aktual'nye problemy zoogeografii i bioraznoobraziya Dal'nego Vostoka Rossii: materialy Vserossijskogo simpoziuma, posvyashchennogo150-letiyu so dnya rozhdeniya V. K. Arsen'eva (Khabarovsk, 29-31 marta 2022 g.) [Actual problems of zoogeography and biodiversity of the Far East of Russia: Proceedings of the All-Russian Symposium devoted to the 150th birthday of V. K. Arseniev (Khabarovsk, March 29-31, 2022)]. Khabarovsk: Biosfera BF Publ., pp. 124-130. (In Russian) Koval'skaya, Yu. M., Sokolov, V. E. (1980) Novyj vid polevok (Rodentia, Cricetidae, Microtus) iz nizhnego Priamur'ya [A new species of vole (Rodentia, Cricetidae, Microtinae) from the lower Amur territory]. Zoologicheskij zhurnal, vol. 59, no. 9, pp. 1409-1416. (In Russian) Sheremetyeva, I. N., Kartavtseva, I. V., Vasiljeva, T. V. (2017a) Does Alexandromys evoronensis inhabit the northeastern part of Verkhnezeiskaya Plain? Biology Bulletin, vol. 44, no. 9, pp. 1151-1157. https://doi.org/10.1134/S1062359017090126 (In English). Sheremetyeva, I. N, Kartavtseva, I. V, Vasiljeva, T. V., Frisman, L. V. (2017b) Voles of the genus Alexandromys from the Verkhnebureinskaya Depression. Biology Bulletin, vol. 44, no. 7, pp. 813819. https://doi.org/10.1134/S1062359017070159 (In English) Sheremetyeva, I. N, Kartavtseva, I. V, Frisman, L. V. (2023) Polimorfizm i differentsiatsiya trekh populyatsij evoronskoj polevki po dannym izmenchivosti Kontrol'nogo regiona mitokhondrial'noj DNK [Polymorphism and differentiation of the Evoron vole three populations according to the mtDNA control region variability]. Genetica, vol. 44, no. 2, pp. 157-169. (In Russian)

For citation: Kartavtseva, I. V., Stepanova, A. I., Sheremetyeva, I. N., Pavlenko, M. V., Frisman, L. V. (2023) A new record of the Evoron vole (Rodentia, Arvicolinae: Alexandromys evoronensis) in the Far East. Amurian Zoological Journal, vol. XV, no. 2, pp. 378-384. https://www.doi.org/10.33910/2686-9519-2023-15-2-378-384

Received 22 March 2023; reviewed 15 April 2023; accepted 25 April 2023.

Для цитирования: Картавцева, И. В., Степанова, А. И., Шереметьева, И. Н., Павленко, М. В., Фрисман, Л. В. (2023) Новая находка эворонской полевки Alexandromys evoronensis (Rodentia, Arvicolinae) на Дальнем Востоке. Амурский зоологический журнал, т. XV, № 2, с. 378-384. https://www.doi.org/10.33910/2686-9519-2023-15-2-378-384

Получена 22 марта 2023; прошла рецензирование 15 апреля 2023; принята 25 апреля 2023.