Промышленный меланизм бабочек получил генетическое объяснение

Рис. 1. Восхитительные узоры на крыльях бабочек складываются из отдельных чешуек, различающихся по цвету, форме и строению. Окраска одних чешуек определяется пигментами, других — тонкослойной интерференцией. Каждая чешуйка одноцветна и образуется единственной клеткой. Фото Linden Gledhill с сайта notcot.com

Промышленный меланизм березовой пяденицы давно вошел в учебники как яркий пример эволюции в действии. Однако до сих пор не была известна природа мутации, породившей черную (меланистическую) форму березовой пяденицы, распространившуюся в индустриальных районах в связи с потемнением стволов деревьев. Британские генетики показали, что появление темных бабочек было связано со встраиванием транспозона в ген cortex, регулирующий деление клеток. Одновременно другая группа исследователей обнаружила, что варианты (аллели) этого гена коррелируют с различными элементами орнамента у самых разных бабочек. Судя по всему, ген cortex был привлечен к раскрашиванию крыльев еще на заре эволюции бабочек. Каким образом регулятор клеточных делений управляет окраской крыльев, пока неясно.

Черная форма carbonaria березовой пяденицы Biston betularia впервые была зарегистрирована в Манчестере в 1848 году. В дальнейшем она стала быстро распространяться. Во время промышленной революции в Англии из-за загрязнения воздуха резко сократилось количество лишайников на стволах деревьев. Поэтому бабочки исходной, светлой формы (typica), незаметные на фоне светлых лишайников, стали бросаться в глаза на темной голой коре. Избирательное выедание птицами светлых бабочек привело к тому, что частота встречаемости формы carbonaria в промышленных районах Англии выросла от 0 до 99%. Но триумф черных бабочек был недолгим: в 1960–1970-е годы борьба с загрязнением воздуха стала приносить ощутимые плоды, и лишайники постепенно вернулись на стволы деревьев. Частота встречаемости формы carbonaria начала снижаться и к настоящему времени упала до 5%. Аналогичные процессы на фоне индустриализации происходили с несколькими десятками видов бабочек в разных странах.

Промышленный меланизм березовой пяденицы давно вошел в учебники как типичный пример адаптивных изменений под действием отбора в изменившихся условиях среды. Пожалуй, это вообще самый известный пример наблюдаемой эволюции. При этом, как ни странно, до сих пор не была идентифицирована конкретная мутация, от которой у бабочек почернели крылья. Лишь недавно удалось, комбинируя классические методы генетики (то есть скрещивания и анализ расщепления признаков у потомства) и современные методы секвенирования и анализа нуклеотидных последовательностей, выявить участок генома длиной менее 400 кб (килобаз, тысяч пар оснований), в котором находится искомая мутация. Этот участок включает 13 белок-кодирующих генов и два гена микро-РНК. Удалось также показать, что распространившаяся в популяциях березовой пяденицы доминантная мутация carbonaria возникла единожды и совсем недавно (A. E. van’t Hof et al., 2011. Industrial melanism in British peppered moths has a singular and recent mutational origin). Разумеется, это не значит, что другие мутации, приводящие к меланизму, никогда не возникали. Это значит лишь, что данный конкретный случай промышленного меланизма у данного вида бабочек был связан с распространением только одной такой мутации, возникшей недавно.

Британские генетики, получившие этот результат, не остановились на достигнутом. В своей новой статье, опубликованной в последнем выпуске журнала Nature, они сообщили об успешной расшифровке молекулярной природы мутации carbonaria. Для этого пришлось тщательно отсеквенировать упомянутый участок генома у 110 черных и 283 светлых особей Biston betularia.

Оказалось, что полиморфизмы (различия нуклеотидной последовательности), коррелирующие с окраской крыльев, концентрируются только в одном из 13 генов, а именно в гене cortex. В пределах этого гена таких полиморфизмов оказалось довольно много, но только один из них встречается исключительно у черных бабочек (у 105 особей из 110) и не был встречен ни у одной светлой особи. Очевидно, именно этот полиморфизм и является искомой мутацией carbonaria, а все остальные полиморфизмы, чаще встречающиеся у черных бабочек, чем у светлых, распространились вместе с ним за счет сцепленного наследования (генетического автостопа, см. Genetic hitchhiking).

Природа мутации carbonaria оказалась весьма интересной: это не что иное, как крупный (21 925 нуклеотидов) мобильный элемент (транспозон), встроившийся в первый интрон гена cortex (рис. 2). Таким образом, получено еще одно наглядное подтверждение способности транспозонов производить полезные наследственные изменения (разумеется, полезность и вредность мутаций зависят от условий, и мутация carbonaria была полезна лишь в условиях сильного промышленного загрязнения).

Промышленный меланизм бабочек получил генетическое объяснение

Рис. 2. Структура гена cortex у черной и светлой форм березовой пяденицы (вверху) и фрагмент этого гена, в который у черных бабочек встроен транспозон (внизу). Пронумерованные вертикальные штрихи (1A, 1B, 2–9) обозначают экзоны. Черные вертикальные линии на фоне горизонтальной серой полосы показывают расположение полиморфизмов, коррелирующих с черной окраской. Сам транспозон состоит из участка длиной 9 кб (тысяч пар оснований), повторенного 2,3 раза (RU — repeat unit). Характерная «роспись», по которой можно безошибочно распознать ДНК-транспозон класса II, перемещающийся методом «cut-and-paste», — это обращенные концевые повторы (TGTAAC…GTTACA, выделены красным), являющиеся неотъемлемой функциональной частью транспозона, и прямые повторы (CCTC…CCTC), которые образуются как побочный результат встраивания транспозона в хозяйский геном. Рисунок из обсуждаемой статьи A. E. van’t Hof et al. в Nature

Авторы показали, что встраивание транспозона привело к усилению экспрессии гена cortex на той стадии развития личинки, когда происходит наиболее интенсивный рост зачатков крыльев. Ген имеет две альтернативные точки начала транскрипции (1A и 1B на рис. 2), поэтому на его основе синтезируется два варианта (изоформы) белка. Как выяснилось, встроенный транспозон усиливает экспрессию только одной из двух изоформ, более массовой (1B).

Анализ распределения полиморфизмов в окрестностях ключевой мутации подтвердил, что мутация carbonaria возникла недавно (скорее всего, в первой половине XIX века) и быстро распространилась под действием отбора. Хотя эпоха грязного воздуха, давшая преимущество черным бабочкам, длилась недолго, их короткий триумф оставил в их геномах характерные следы (см. Selective sweep). Чем ближе к месту встройки транспозона, тем чаще в пределах гена cortex у черных бабочек встречаются строго определенные полиморфизмы — те самые, которые имелись у счастливой первой обладательницы мутации carbonaria и затем распространились за счет генетического автостопа.

Что касается тех пяти черных бабочек, у которых нет транспозона в интроне гена cortex, то это, судя по всему, носители альтернативных аллелей того же гена, которые обычно обеспечивают вариант окраски insularia, промежуточный между typica и carbonaria. Ранее уже было известно, что аллели insularia изредка порождают очень темные фенотипы, практически неотличимые от carbonaria.

В том же выпуске Nature опубликована статья другого, более многочисленного международного исследовательского коллектива, в которой показана ведущая роль гена cortex в эволюции окраски крыльев у ряда других бабочек (рис. 3). Основное внимание в этом исследовании было уделено тропическим бабочкам рода Heliconius, у которых широко распространена мимикрия, а окраска крыльев крайне разнообразна (см. Зафиксирован начальный этап видообразования у тропических бабочек, «Элементы», 09.11.2009).

Промышленный меланизм бабочек получил генетическое объяснение

Рис. 3. Один и тот же участок генома обеспечивает вариации окраски у разных бабочек. Справа — схема хромосомы, на которой разными цветами обозначены гомологичные участки, а серым выделен фрагмент, содержащий ген cortex, изменения которого влияют на окраску крыльев. У Heliconius erato данный локус контролирует наличие или отсутствие желтой полосы на задних крыльях, у H. melpomene — желтые полосы на обеих парах крыльев, у H. numata — черные, желтые и оранжевые элементы узора, обеспечивающие сходство с бабочками рода Melinaea (пример мимикрии). Рисунок из обсуждаемой статьи N. J. Nadeau et al. в Nature

Оказалось, что у разных видов Heliconius самые разнообразные элементы орнамента крыльев — черные, желтые, оранжевые пятна и полосы — коррелируют с полиморфизмами в гене cortex (рис. 3). Как правило, ключевые полиморфизмы находятся в некодирующих областях гена, в том числе в интронах. Это значит, что эволюционные изменения орнамента крыльев были связаны с изменениями регуляции гена cortex, а не структуры кодируемого им белка. По-видимому, в некоторых случаях полиморфизмы, связанные с окраской крыльев, влияют на альтернативный сплайсинг, которому подвергается cortex, и меняют уровень экспрессии и соотношение изоформ в зачатках крыльев.

Ген cortex не относится к числу генов, которые можно было заподозрить в причастности к раскраске крыльев. Он входит в семейство генов, регулирующих деление клеток. Гены этого семейства активируют комплекс стимуляции анафазы, что способствует разделению сестринских хромосом во время клеточного деления. У дрозофилы ген cortex задействован в регуляции мейоза в яичниках самки и не имеет никакого отношения к окраске крыльев. Авторы второй статьи проверили, что будет, если ген cortex бабочки Heliconius melpomene заставить работать в зачатках крыльев дрозофилы — и это не привело ни к какому видимому эффекту.

Судя по всему, ген cortex, изначально не связанный с окраской, был привлечен к работе над орнаментом крыльев около 100 млн лет назад, на заре эволюции бабочек, и с тех пор неоднократно подвергался интенсивному отбору в разных эволюционных линиях.

Таким образом, генетические основы эволюции узоров на крыльях бабочек постепенно проясняются. Мы уже знаем, что в формировании узоров задействованы сигнальные белки и регуляторы транскрипции, которые обычно (у других животных, да и у тех же бабочек) выполняют совершенно другие функции. Увлекательный рассказ об этих исследованиях читатель найдет в главе 8 книги Шона Кэрролла «Бесконечное число самых прекрасных форм». Например, за красные пятна на крыльях Heliconius отвечает ген optix, важнейший регулятор развития глаз (см. Найден ген, отвечающий за эволюцию окраски у бабочек, «Элементы», 31.08.2011). В центре будущих ярких круглых пятен (глазков), например, у бабочек Bicyclus (см.: Самцы и самки меняются ролями при смене погоды, «Элементы», 27.12.2012), экспрессируется ген distal-less (dll), участвующий в закладке конечностей — да и вообще любых отростков тела — у самых разных животных. Что общего между глазом насекомого и красным пятном на крыле? Разве что красный пигмент, но эта связь скорее всего случайна. Что общего между глазком на крыле и ногой? Здесь связь может оказаться более существенной: и то, и другое в ходе развития возникает сначала как некий кружочек, «нарисованный» в определенном месте развивающегося организма экспрессией сигнального белка, который производится в центре кружка.

Ген cortex отличается от найденных ранее генов орнаментации крыльев бабочек тем, что он кодирует не транскрипционный фактор и не сигнальный белок, выделяемый клетками наружу для межклеточного общения. Транскрипционные факторы и сигнальные белки легко приобретают новые функции: это профессиональные переключатели и регуляторы работы генов, которым всё равно, какие гены регулировать. Но cortex — специфический регулятор клеточных делений, который у дрозофилы обслуживает процесс созревания яйцеклеток. Его вовлеченность в раскрашивание крыльев бабочек приоткрывает какие-то новые грани в эволюционной биологии развития. Каким образом cortex влияет на окраску крыльев, неясно. Однако нужно иметь в виду, что узор на крыльях бабочек сложен из чешуек, каждая из которых формируется из единственной клетки (рис. 1). Динамика процессов деления и миграции клеток, которым суждено стать чешуйками того или иного цвета, на стадии поздней личинки и куколки, очевидно, влияет на итоговый орнамент, но конкретные механизмы этого влияния еще предстоит выяснить.

Источник: elementy.ru

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  370. I’m developing a new blog about literature (what I’ve read, what I read), yet I’m having problem thinking about a title. I like the concept of something relating to a fascination with literature however I believe bookophilia is on the average side. What do you think about Litophilia? Is it as well similar to «lithophilia» Which means the love of stones? Any kind of ideas? Many thanks!.

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  586. On my friend’s blogs they have included me on their blog site rolls, however my own always rests at the end of the list and does not listing when I upload like it does for others. Is this a setting that I need to change or is this a selection that they have made?.

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  607. What are some excellent Tumblr blog sites that enable you to submit images, to get even more fans?

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